Coral Reefs

, Volume 29, Issue 4, pp 929–939

Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide

Report

Abstract

Complex environmental cues dictate the settlement of coral planulae in situ; however, simple artificial cues may be all that is required to induce settlement of ex situ larval cultures for reef re-seeding and restoration projects. Neuropeptides that transmit settlement signals and initiate the metamorphic cascade have been isolated from hydrozoan taxa and shown to induce metamorphosis of reef-building Acropora spp. in the Indo-Pacific, providing a reliable and efficient settlement cue. Here, the metamorphic activity of six GLW-amide cnidarian neuropeptides was tested on larvae of the Caribbean corals Acropora palmata, Montastraea faveolata and Favia fragum. A. palmata planulae were induced to settle by the exogenous application of the neuropeptide Hym-248 (concentrations ≥1 × 10−6 M), achieving 40–80% attachment and 100% metamorphosis of competent planulae (≥6 days post-fertilization) during two spawning seasons; the remaining neuropeptides exhibited no activity. Hym-248 exposure rapidly altered larval swimming behavior (<1 h) and resulted in >96% metamorphosis after 6 h. In contrast, M. faveolata and F. fragum planulae did not respond to any GLW-amides tested, suggesting a high specificity of neuropeptide activators on lower taxonomic scales in corals. Subsequent experiments for A. palmata revealed that (1) the presence of a biofilm did not enhance attachment efficiency when coupled with Hym-248 treatment, (2) neuropeptide-induced settlement had no negative effects on early life-history developmental processes: zooxanthellae acquisition and skeletal secretion occurred within 12 days, colonial growth occurred within 36 days, and (3) Hym-248 solutions maintained metamorphic activity following storage at room temperature (10 days), indicating its utility in remote field settings. These results corroborate previous studies on Indo-Pacific Acropora spp. and extend the known metamorphic activity of Hym-248 to Caribbean acroporids. Hym-248 allows for directed and reliable settlement of larval cultures and has broad applications to the study and rehabilitation of threatened Acropora populations in the Caribbean.

Keywords

Acropora palmata Caribbean coral reefs Restoration Settlement Metamorphosis Neuropeptides 

References

  1. Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441–450CrossRefGoogle Scholar
  2. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571CrossRefGoogle Scholar
  3. Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17:2796–2811CrossRefPubMedGoogle Scholar
  4. Becker LC, Mueller E (2001) The culture, transplantation and storage of Montastraea faveolata, Acropora cervicornis and Acropora palmata: what we have learned so far. Bull Mar Sci 69:881–896Google Scholar
  5. Bruckner AW (2002) Proceedings of the Caribbean Acropora workshop: potential application of the US Endangered Species Act as a conservation strategy. NOAA Technical Memorandum. NMFS-OPR-24, Silver Spring, MarylandGoogle Scholar
  6. Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98:5067–5071CrossRefPubMedGoogle Scholar
  7. Erwin PM, Song B, Szmant AM (2009) Settlement behavior of Acropora palmata planulae: effects of biofilm age and crustose coralline algae. Proc 11th Int Coral Reef Symp 1219–1224Google Scholar
  8. Golbuu Y, Richmond RH (2007) Substratum preferences in planulae larvae of two species of scleractinian corals, Goniastrea retiformis and Stylaraea punctata. Mar Biol 152:639–644CrossRefGoogle Scholar
  9. Grimmelikhuijzen JP, Williamson M, Hansen GN (2002) Neuropeptides in cnidarians. Can J Zool 80:1690–1702CrossRefGoogle Scholar
  10. Harrington L, Fabricius K, De’ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437CrossRefGoogle Scholar
  11. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky (ed) Ecosystems of the world, vol 25, coral reefs. Elsevier Science Publishers, Amsterdam, pp 133–207Google Scholar
  12. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189CrossRefPubMedGoogle Scholar
  13. Hatta M, Iwao K (2003) Metamorphosis induction and its possible application to coral seedlings production. In: Sexena N (ed) Recent advances in marine science and technology, 2002. Japan International Science and Technology Federation Akaskak, Tokyo, pp 465–470Google Scholar
  14. Hatta M, Iwao K, Taniguchi H, Omori M (2004) Restoration technology using sexual reproduction. In: Omori M, Fujiwara S (eds) Manual for restoration and remediation of coral reefs. Nature Conservation Bureau, Ministry of the Environment, Japan, pp 14–28Google Scholar
  15. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279CrossRefGoogle Scholar
  16. Heyward AJ, Smith LD, Rees M, Field SN (2002) Enhancement of coral recruitment by in situ mass culture of coral larvae. Mar Ecol Prog Ser 230:113–118CrossRefGoogle Scholar
  17. Hirose M, Yamamoto H, Nonaka M (2008) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27:247–254CrossRefGoogle Scholar
  18. Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129Google Scholar
  19. Katsukura Y, David CN, Grimmelikhuijzen CJP, Sugiyama T (2003) Inhibition of metamorphosis by RFamide neuropeptides in planulae larvae of Hydractinia echinata. Dev Genes Evol 213:579–586CrossRefPubMedGoogle Scholar
  20. Leitz T, Morand K, Mann M (1994) Metamorphosin A, a novel peptide controlling development of the lower metazoan Hyrdactinia echinata. Dev Biol 163:440–446CrossRefPubMedGoogle Scholar
  21. Leviev I, Williamson M, Grimmelikhuijzen CJP (1997) Molecular cloning of a preprohormone from Hydra magnipapillata containing multiple copies of Hydra-LWamide (Leu-Trp-NH2) neuropeptides: evidence for processing at Ser and Asn residues. J Neurochem 68:1319–1325CrossRefPubMedGoogle Scholar
  22. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, Colbourne JK, Willis BL, Matz MV (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10:219CrossRefPubMedGoogle Scholar
  23. Miller K, Mundy C (2003) Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22:99–106CrossRefGoogle Scholar
  24. Miller MW, Szmant AM (2006) Lessons learned from experimental key-species restoration. In: Precht WF (ed) Coral reef restoration handbook: the rehabilitation of an ecosystem under seige. CRC Press, Boca Raton, FL, pp 219–234Google Scholar
  25. Morse DE, Hooker N, Morse ANC, Jensen R (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217CrossRefGoogle Scholar
  26. Morse ANC, Iwao K, Baba M, Shimoike K, Hayashibara T, Omori M (1996) An ancient chemosensory mechanism brings new life to coral reefs. Biol Bull 191:149–154CrossRefGoogle Scholar
  27. Müller WA, Leitz T (2002) Metamorphosis in the Cnidaria. Can J Zool 80:1755–1771CrossRefGoogle Scholar
  28. Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131CrossRefGoogle Scholar
  29. NMFS (2006) Endangered and threatened species: final listing determinations for Elkhorn coral and Staghorn coral. Federal Register 71:26852–26861Google Scholar
  30. Nozawa Y (2008) Micro-crevice structure enhances coral spat survivorship. J Exp Mar Biol Ecol 367:127–130CrossRefGoogle Scholar
  31. Nugues MM, Szmant AM (2006) Coral settlement onto Halimeda opuntia: a fatal attraction to an ephemeral substrate? Coral Reefs 25:585–591CrossRefGoogle Scholar
  32. Okubo N, Taniguchi H, Motokawa T (2005) Successful methods for transplanting fragments of Acropora formosa and Acropora hyacinthus. Coral Reefs 24:333–342CrossRefGoogle Scholar
  33. Omori M, Fujiwara S (2004) Manual for restoration and remediation of coral reefs. Nature Conservation Bureau, Ministry of the Environment, JapanGoogle Scholar
  34. Omori M, Iwao K, Tamura M (2008) Growth of transplanted Acropora tenuis 2 years after egg culture. Coral Reefs 27:165CrossRefGoogle Scholar
  35. Petersen D, Laterveer M, Schuhmacher H (2005a) Spatial and temporal variation in larval settlement of reefbuilding corals in mariculture. Aquaculture 249:317–327CrossRefGoogle Scholar
  36. Petersen D, Hatta M, Laterveer M, van Bergen D (2005b) Ex situ transportation of coral larvae for research, conservation and aquaculture. Coral Reefs 24:510–513CrossRefGoogle Scholar
  37. Petersen D, Laterveer M, Carl M, Borneman E, Brittsan M, Hagedorn M, Schick M (2008) Noah’s Ark for the threatened Elkhorn coral Acropora palmata. Coral Reefs 27:715CrossRefGoogle Scholar
  38. Randall CR, Szmant AM (2009) Elevated temperature affects development, survivorship, and settlement of the Elkhorn Coral, Acropora palmata (Lamarck 1816). Biol Bull 217:269–282PubMedGoogle Scholar
  39. Richmond RH (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 175–197Google Scholar
  40. Rinkevich B (2005) Conservation of coral reefs through active restoration measures: recent approaches and last decade progress. Environ Sci Technol 39:4333–4342CrossRefPubMedGoogle Scholar
  41. Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij M, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithsonian Contrib Mar Sci 38:437–457Google Scholar
  42. Ritson-Williams R, Paul VJ, Arnold SN, Steneck RS (2010) Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29:71–81CrossRefGoogle Scholar
  43. Sammarco PW (1980) Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. J Exp Mar Biol Ecol 45:245–272CrossRefGoogle Scholar
  44. Sammarco PW, Carleton JH (1981) Damselfish territoriality and coral community structure: reduced grazing, coral recruitment, and effects on coral spat. Proc 4th Int Coral Reef Symp 2:525–535Google Scholar
  45. Schmich J, Trepel S, Leitz T (1998) The role of GLWamides in metamorphosis of Hydractinia echinata. Dev Genes Evol 208:267–273CrossRefPubMedGoogle Scholar
  46. Schwarz JA, Brokstein PB, Voolstra C, Terry AY, Miller DJ, Szmant AM, Coffroth MA, Medina M (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9:97CrossRefPubMedGoogle Scholar
  47. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54CrossRefGoogle Scholar
  48. Szmant AM, Meadows MG (2006) Developmental changes in coral larval buoyancy and vertical swimming behavior: implications for dispersal and connectivity. Proc 10th Int Coral Reef Symp 1:431–437Google Scholar
  49. Szmant AM, Miller MW (2006) Settlement preferences and post-settlement mortality of laboratory cultured and settled larvae of the Caribbean hermatypic corals Montastraea faveolata and Acropora palmata in the Florida Keys, USA. Proc 10th Int Coral Reef Symp 1:43–49Google Scholar
  50. Takahashi T, Muneoka Y, Lohmann J, Lopez de Haro MS, Solleder G, Bosch TCG, David CN, Bode HR, Koizumi O, Shimizu H, Hatta M, Fujisawa T, Sugiyama T (1997) Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families. Proc Natl Acad Sci USA 94:1241–1246CrossRefPubMedGoogle Scholar
  51. Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TCG, Kobayakawa Y, Mohri S, Bode HR, Yum S, Hatta M, Fujisawa T (2000) A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development 127:997–1005PubMedGoogle Scholar
  52. Takahashi T, Kobayakawa Y, Muneoka Y, Fujisawa Y, Mohri S, Hatta M, Shimizu H, Fujisawa T, Sugiyama T, Takahara M, Yanagi K, Koizumi O (2003) Identification of a new member of the GLWamide peptide family: physiology activity and cellular localization in cnidarian polyps. Comp Biochem Physiology Part B 135:309–324CrossRefGoogle Scholar
  53. Takahashi T, Hayakawa E, Koizumi O, Fujisawa T (2008) Neuropeptides and their function in Hydra. Acta Biol Hung 59:227–235CrossRefPubMedGoogle Scholar
  54. Van Oppen MJH, McDonald BJ, Willis B, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18:1315–1329PubMedGoogle Scholar
  55. Vandermeulen JH (1974) Studies of reef corals, II, fine structure of planktonic planulae larva of Pocillopora damicornis, with emphasis on the aboral epidermis. Mar Biol 27:239–249CrossRefGoogle Scholar
  56. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, Szmant AM, Coffroth MA, Medina M (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18:1823–1833CrossRefPubMedGoogle Scholar
  57. Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, Blackall LL, Negri AP (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70:1213–1221CrossRefPubMedGoogle Scholar
  58. Wilkinson CR (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, AustraliaGoogle Scholar
  59. Yeemin T, Suttacheep M, Pettongma R (2006) Coral reef restoration projects in Thailand. Ocean Coast Manage 49:562–575CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA
  2. 2.Centre d’Estudis Avançats de Blanes (CEAB, CSIC)Blanes (Girona)Spain

Personalised recommendations